Extracellular biogenic nanomaterials inhibit pyoverdine production in Pseudomonas aeruginosa: a novel insight into impacts of metal(loid)s on environmental bacteria

Applied Microbiology and Biotechnology

Volumn 99, Issue 4, 2015, Pages 1957-1966

  Mohanty, Anee ^a,b   Liu, Yang ^a   Yang, Liang ^a,c   Cao, Bin ^a,b  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Biofilm; Econanotoxicity; Nanomaterial; Pseudomonas aeruginosa; Shewanella oneidensis; Siderophore

Indexed keywords

BIOCHEMISTRY; BIOFILMS; ECOSYSTEMS; ENVIRONMENTAL IMPACT; METALS; NANOSTRUCTURED MATERIALS; SMELTING; TELLURIUM COMPOUNDS;

ANTHROPOGENIC ACTIVITY; ECONANOTOXICITY; ENVIRONMENTAL ORGANISMS; METAL-REDUCING BACTERIA; PSEUDOMONAS AERUGINOSA; SHEWANELLA ONEIDENSIS; SIDEROPHORE PRODUCTION; SIDEROPHORES;

BACTERIA;

BIOGENIC NANOMATERIAL; NANOMATERIAL; PYOVERDINE; SIDEROPHORE; UNCLASSIFIED DRUG; METALLOID; OLIGOPEPTIDE; TELLURIUM;

ARTICLE; BIOFILM; BIOSYNTHESIS; CONTROLLED STUDY; FUNGUS CULTURE; GENE EXPRESSION; MICROBIAL COMMUNITY; NONHUMAN; PSEUDOMONAS AERUGINOSA; TRANSCRIPTOMICS; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, BACTERIAL; METALLOIDS; NANOSTRUCTURES; OLIGOPEPTIDES; PSEUDOMONAS AERUGINOSA; TELLURIUM;

EID: 84925488777     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6097-5     Document Type: Article

References (62)

1. Buckling A, Harrison F, Vos M, Brockhurst MA, Gardner A, West SA, Griffin A (2007) Siderophore-mediated cooperation and virulence in Pseudomonas aeruginosa. FEMS Microbiol Ecol 62(2):135–141
2. Cao B, Ahmed B, Kennedy DW, Wang Z, Shi L, Marshall MJ, Fredrickson JK, Isern NG, Majors PD, Beyenal H (2011) Contribution of extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms to U (VI) immobilization. Environ Sci Technol 45(13):5483–5490
3. Cao B, Majors PD, Ahmed B, Renslow RS, Silvia CP, Shi L, Kjelleberg S, Fredrickson JK, Beyenal H (2012) Biofilm shows spatially stratified metabolic responses to contaminant exposure. Environ Microbiol 14(11):2901–2910
4. Chen C-Y, Nace G, Irwin P (2003) A 6x6 drop plate method for simultaneous colony counting and MPN enumeration of Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli. J Microbiol Methods 55:475–479
5. Chua SL, Tan SY, Rybtke MT, Chen Y, Rice SA, Kjelleberg S, Tolker-Nielsen T, Yang L, Givskov M (2013) Bis-(3′-5′)-cyclic dimeric GMP regulates antimicrobial peptide resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 57(5):2066–2075
6. Cordero OX, Ventouras L-A, DeLong EF, Polz MF (2012) Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc Natl Acad Sci U S A 109(49):20059–20064
7. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49(1):711–745
8. Crusz S, Popat R, Rybtke M, Camara M, Givskov M, Tolker-Nielsen T, Diggle S, Williams P (2012) Bursting the bubble on bacterial biofilms: a flow cell methodology. Biofouling 28(8):835–842
9. Ding Y, Peng N, Du Y, Ji L, Cao B (2014) Disruption of putrescine biosynthesis in Shewanella oneidensis enhances biofilm cohesiveness and performance in Cr (VI) immobilization. Appl Environ Microbiol 80(4):1498–1506
10. Dopp E, Hartmann LM, Florea AM, Rettenmeier AW, Hirner AV (2004) Environmental distribution, analysis, and toxicity of organometal(loid) compounds. Crit Rev Toxicol 34(3):301–333
11. Drenkard E (2003) Antimicrobial resistance of Pseudomonas aeruginosa biofilms. Microbes Infect 5(13):1213–1219
12. Greenwald J, Hoegy F, Nader M, Journet L, Mislin GL, Graumann PL, Schalk IJ (2007) Real time fluorescent resonance energy transfer visualization of ferric pyoverdine uptake in Pseudomonas aeruginosa. A role for ferrous iron. J Biol Chem 282(5):2987–2995
13. Gristina AG, Hobgood CD, Webb LX, Myrvik QN (1987) Adhesive colonization of biomaterials and antibiotic resistance. Biomaterials 8(6):423–426
14. Habimana O, Steenkeste K, Fontaine-Aupart MP, Bellon-Fontaine MN, Kulakauskas S, Briandet R (2011) Diffusion of nanoparticles in biofilms is altered by bacterial cell wall hydrophobicity. Appl Environ Microbiol 77(1):367–368
15. Han X, Gu JD (2010) Sorption and transformation of toxic metals by microorganisms. In: Mitchell R, Gu J (eds) Environ microbiol, 2nd edn. Willy, New York, pp 153–176
16. Hannauer M, Yeterian E, Martin LW, Lamont IL, Schalk IJ (2010) An efflux pump is involved in secretion of newly synthesized siderophore by Pseudomonas aeruginosa. FEBS Lett 584(23):4751–4755
17. Harrison F, Paul J, Massey RC, Buckling A (2007) Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. ISME J 2(1):49–55
18. Hockin SL, Gadd GM (2003) Linked redox precipitation of sulfur and selenium under anaerobic conditions by sulfate-reducing bacterial biofilms. Appl Environ Microbiol 69(12):7063–7072
19. Kalathil S, Lee J, Cho M (2011) Electrochemically active biofilm-mediated synthesis of silver nanoparticles in water. Green Chem 13:1482–1485
20. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK (2007) The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 117(4):877–888
21. Kim D-H, Kanaly R, Hur HG (2012) Biological accumulation of tellurium nanorod structures via reduction of tellurite by Shewanella oneidensis MR-1. Bioresour Technol 125:127–131
22. Klonowska A, Heulin T, Vermeglio A (2005) Selenite and tellurite reduction by Shewanella oneidensis. Appl Environ Microbiol 71(9):5607–5609
23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods (San Diego, Calif) 25(4):402–408
24. Mohanty A, Kathawala MH, Zhang J, Chen WN, Loo JSC, Kjelleberg S, Yang L, Cao B (2014a) Biogenic tellurium nanorods as a novel antivirulence agent inhibiting pyoverdine production in Pseudomonas aeruginosa. Biotechnol Bioeng 111(5):858–865
25. Mohanty A, Wu Y, Cao B (2014b) Impacts of engineered nanomaterials on microbial community structure and function in natural and engineered ecosystems. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-6000-4
26. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628
27. Moscoso H, Saavedra C, Loyola C, Pichuantes S, Vasquez C (1998) Biochemical characterization of tellurite-reducing activities of Bacillus stearothermophilus V. Res Microbiol 149(6):389–397
28. Narayanan KB, Sakthivel N (2010) Biological synthesis of metal nanoparticles by microbes. Adv Colloid Interf Sci 156(1–2):1–13
29. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270(45):26723–26726
30. Ng CK, Sivakumar K, Liu X, Madhaiyan M, Ji L, Yang L, Tang C, Song H, Kjelleberg S, Cao B (2013) Influence of outer membrane c-type cytochromes on particle size and activity of extracellular nanoparticles produced by Shewanella oneidensis. Biotechnol Bioeng 110(7):1831–1837
31. Peek ME, Bhatnagar A, McCarty NA, Zughaier SM (2012) Pyoverdine, the major siderophore in Pseudomonas aeruginosa, evades NGAL recognition. Interdiscip Perspect Infect Dis 2012:10
32. Peralta-Videa JR, Zhao LJ, Lopez-Moreno ML, de la Rosa G, Hong J, Gardea-Torresdey JL (2011) Nanomaterials and the environment: a review for the biennium 2008–2010. J Hazard Mater 186(1):1–15
33. Peulen T-O, Wilkinson KJ (2011) Diffusion of nanoparticles in a biofilm. Environ Sci Technol 45(8):3367–3373
34. Prosser BL, Taylor D, Dix BA, Cleeland R (1987) Method of evaluating effects of antibiotics on bacterial biofilm. Antimicrob Agents Chemother 31(10):1502–1506
35. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28(3):142–149
36. Saha R, Saha N, Donofrio RS, Bestervelt LL (2013) Microbial siderophores: a mini review. J Basic Microbiol 53(4):303–317
37. Schalk IJ, Guillon L (2013) Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol 15(6):1661–1673
38. Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13(11):2844–2854
39. Schofield EJ, Veeramani H, Sharp JO, Suvorova E, Bernier-Latmani R, Mehta A, Stahlman J, Webb SM, Clark DL, Conradson SD (2008) Structure of biogenic uraninite produced by Shewanella oneidensis strain MR-1. Environ Sci Technol 42(21):7898–7904
40. 2 for thin film solar cell applications. Sol Energy Mater Sol Cells 82(1):315–330
41. Sintubin L, Verstraete W, Boon N (2012) Biologically produced nanosilver: current state and future perspectives. Biotechnol Bioeng 109(10):2422–2436
42. Sivakumar K, Wang VB, Chen X, Bazan GC, Kjelleberg S, Loo SCJ, Cao B (2014) Membrane permeabilization underlies the enhancement of extracellular bioactivity in Shewanella oneidensis by a membrane-spanning conjugated oligoelectrolyte. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-5973-3
43. Staupendahl G, Schindler K (1982) Optical tuning of a tellurium cavity: optical modulation and bistability in the infrared region at room temperature. Opt Quant Electron 14(2):157–167
44. Stewart PS (1996) Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob Agents Chemother 40(11):2517–2522
45. Stewart PS (2003) Diffusion in biofilms. J Bacteriol 185(5):1485–1491
46. Stewart PS, William Costerton J (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358(9276):135–138
47. Stoodley P, Sauer K, Davies D, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56(1):187–209
48. Suzuki Y, Kelly SD, Kemner KM, Banfield JF (2002) Radionuclide contamination: nanometre-size products of uranium bioreduction. Nature 419(6903):134
49. Trutko SM, Akimenko VK, Suzina NE, Anisimova LA, Shlyapnikov MG, Baskunov BP, Duda VI, Boronin AM (2000) Involvement of the respiratory chain of gram-negative bacteria in the reduction of tellurite. Arch Microbiol 173(3):178–186
50. 2 gas sensor. Sensors Actuators B Chem 73(1):35–39
51. Turner RJ, Borghese R, Zannoni D (2012) Microbial processing of tellurium as a tool in biotechnology. Biotechnol Adv 30(5):954–963
52. Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15(1):22–30
53. Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647
54. West SA, Buckling A (2003) Cooperation, virulence and siderophore production in bacterial parasites. Proc R Soc Lond [Biol] 270(1510):37–44
55. Winkelmann G, Drechsel H (2001) Microbial siderophores. In: Rehm H.-J, Reed G (eds) Biotechnology set, 2nd edn. Wiley-VCH Verlag GmbH, Weinheim, doi:10.1002/9783527620999.ch5g
56. Xie YP, He YP, Irwin PL, Jin T, Shi XM (2011) Antibacterial activity and mechanism of action of zinc oxide nanoparticles against Campylobacter jejuni. Appl Environl Microbiol 77(7):2325–2331
57. Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, Tolker-Nielsen T (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153(5):1318–1328
58. Yang L, Nilsson M, Gjermansen M, Givskov M, Tolker-Nielsen T (2009) Pyoverdine and PQS mediated subpopulation interactions involved in Pseudomonas aeruginosa biofilm formation. Mol Microbiol 74(6):1380–1392
59. Yeterian E, Martin LW, Guillon L, Journet L, Lamont IL, Schalk IJ (2010) Synthesis of the siderophore pyoverdine in Pseudomonas aeruginosa involves a periplasmic maturation. Amino Acids 38(5):1447–1459
60. Yurkov V, Jappé J, Verméglio A (1996) Tellurite resistance and reduction by obligately aerobic photosynthetic bacteria. Appl Environ Microbiol 62(11):4195–4198
61. Zannoni D (2010) Bacterial processing of metalloids as a tool in biotechnology. J Biotechnol 150:S52–S53
62. Zhang Y, Ng CK, Cohen Y, Cao B (2014) Cell growth and protein expression of Shewanella oneidensis in biofilms and hydrogel-entrapped cultures. Mol BioSyst 10(5):1035–1042